Some problems in the study of the origin of neotropical biodiversity using palaeoecological and molecular phylogenetic evidence

This study contends that progress in the understanding of the origin and maintenance of extant neotropical biodiversity by means of empirical evidence is hampered by the persistence of anachronistic conceptual approaches, notably the adherence to closed paradigms or ruling theories. The topic is discussed from three main perspectives: (1) the tendency to shift from one paradigm to another, (2) the use and abuse of broad generalizations from a single or a few case studies and (3) the use of inadequate phylogenetic dating (usually crown dating alone) for a sound appraisal of diversification timing. The origin of neotropical biodiversity is a complex subject that requires an open-minded attitude to be fully captured. The solution proposed is fairly easy, somewhat trivial, and rooted in the classical multiple working hypotheses (MWH) approach. The MWH seeks to explore any explanation possible for observed phenomena and develop every testable hypothesis in relation to their possible causes. The MWH approach promotes thoroughness, suggests lines of inquiry that might otherwise be overlooked and develops the habit of parallel and complex thought that, unfortunately, is not fully developed in the empirical study of neotropical biodiversity.     

Speciation timing and neotropical biodiversity: the Tertiary-Quaternary debate in the light of molecular phylogenetic evidence

The evolutionary origin of extant species in the Neotropics, one of the most biodiverse regions of the world, has been widely debated. One hypothesis is that neotropical species emerged primarily during the Quaternary (the last ~2 million years), favoured by alternating glacial/interglacial climates. An opposite view proposes an older Tertiary origin linked primarily to palaeogeographical changes. Here, a thorough review of the available literature on DNA molecular dating shows that the Tertiary–Quaternary debate no longer makes sense. Indeed, the > 1400 neotropical species whose origin has been dated have appeared in a continual fashion since the late Eocene/early Oligocene (~39 million years before present) to the Quaternary. Palaeogeographical mechanisms of speciation are relatively well accepted, but diversification processes linked to climate are still controversial. These results are important to unravel both the origin of present-day biodiversity patterns at both local and global scales and the genetic and environmental mechanisms involved, which are two crucial aspects for suitable biodiversity conservation strategies.     

Ecological palaeoecology in the neotropical Gran Sabana region: Long-term records of vegetation dynamics as a basis for ecological hypothesis testing

Long-term palaeoecological records are needed to test ecological hypotheses involving time, as short-term observations are of insufficient duration to capture natural variability. In this paper, we review the published palaeoecological evidence for the neotropical Gran Sabana (GS) region, to record the vegetation dynamics and evaluate the potential effects of natural climatic and anthropogenic (notably fire) drivers of change. The time period considered (last 13,000 years) covers major global climate changes and the arrival of humans in the region. The specific points addressed are climate–vegetation equilibrium, reversibility of vegetation changes, the origin of extant biodiversity and endemism patterns and biodiversity conservation in the face of global warming. Vegetation dynamics is reconstructed by pollen analysis and fire incidence is deduced from microscopic charcoal records. Palaeoclimatic inferences are derived from global and regional records using independent physico-chemical evidence to avoid circular reasoning. After analyzing all the long-term records available from both GS uplands and highlands, we conclude that: (1) Upland vegetation (mostly treeless savannas and savanna–forest mosaics, with occasional Mauritia palm swamps) is not in equilibrium with the dominant climates, but largely conditioned by burning practices; (2) a hypothetical natural or “original” vegetation type for these uplands has not been possible to identify due to continuous changes in both climate and human activities during the last 13,000 years; (3) at the time scale studied (millennial), the shift from forest to savanna is abrupt and irreversible due to the existence of tipping points, no matter the cause (natural or anthropogenic); (4) on the contrary, the shift from savanna to palm swamps is reversible at centennial time scales; (5) some of the reconstructed past vegetation types have no modern analogues owing to the individual species response to environmental shifts, leading to variations in community composition; (6) extant biodiversity and endemism patterns are not the result of a long history of topographical isolation, as previously proposed but, rather, the consequence of the action of climatic and palaeogeographic variations; (7) the projected global warming will likely exacerbate the expansion of upland savannas by favouring positive fire-climate feedbacks; (8) in the highlands, extinction by habitat loss will likely affect biodiversity but to a less extent that prognosticated by models based only on present-day climatic features; (9) future highland communities will likely be different to present ones due to the prevalence of individual species responses to global warming; and (10) conservation strategies at individual species level, rather than at community level, are enriched by long-term palaeoecological studies analyzed here. None of these conclusions would have been possible to derive from short-term neoecological observations.     

South American palaeobotany and the origins of neotropical rainforests

Extant neotropical rainforest biomes are characterized by a high diversity and abundance of angiosperm trees and vines, high proportions of entire-margined leaves, high proportions of large leaves (larger than 4500 mm2), high abundance of drip tips and a suite of characteristic dominant families: Sapotaceae, Lauraceae, Leguminosae (Fabaceae), Melastomataceae and Palmae (Arecaceae). Our aim is to define parameters of extant rainforests that will allow their recognition in the fossil record of South America and to evaluate all known South American plant fossil assemblages for first evidence and continued presence of those parameters. We ask when did these critical rainforest characters arise? When did vegetative parameters reach the level of abundance that we see in neotropical forests? Also, when do specific lineages become common in neotropical forests? Our review indicates that evidence of neotropical rainforest is exceedingly rare and equivocal before the Palaeocene. Even in the Palaeocene, the only evidence for tropical rainforest in South America is the appearance of moderately high pollen diversity. By contrast, North American sites provide evidence that rainforest leaf physiognomy was established early in the Palaeocene. By the Eocene in South America, several lines of evidence suggest that neotropical rainforests were diverse, physiognomically recognizable as rainforest and taxonomically allied to modern neotropical rainforests. A mismatch of evidence regarding the age of origin between sites of palaeobotanical high diversity and sites of predicted tropical climates should be reconciled with intensified collecting efforts in South America. We identify several lines of promising research that will help to coalesce previously disparate approaches to the origin, longevity and maintenance of high diversity floras of South America.     

Investigating the timing of origin and evolutionary processes shaping regional species diversity: Insights from simulated data and neotropical butterfly diversification rates

Different diversification scenarios have been proposed to explain the origin of extant biodiversity. However, most existing meta‐analyses of time‐calibrated phylogenies rely on approaches that do not quantitatively test alternative diversification processes. Here, I highlight the shortcomings of using species divergence ranks, which is a method widely used in meta‐analyses. Divergence ranks consist of categorizing cladogenetic events to certain periods of time, typically to either Pleistocene or to pre‐Pleistocene ages. This approach has been claimed to shed light on the origin of most extant species and the timing and dynamics of diversification in any biogeographical region. However, interpretations drawn from such method often confound two fundamental questions in macroevolutionary studies, tempo (timing of evolutionary rate shifts) and mode (“how” and “why” of speciation). By using simulated phylogenies under four diversification scenarios, constant‐rate, diversity‐dependence, high extinction, and high speciation rates in the Pleistocene, I showed that interpretations based on species divergence ranks might have been seriously misleading. Future meta‐analyses of dated phylogenies need to be aware of the impacts of incomplete taxonomic sampling, tree topology, and divergence time uncertainties, as well as they might be benefited by including quantitative tests of alternative diversification models that acknowledge extinction and diversity dependence.     

The Complete Chloroplast Genome of Guadua angustifolia and Comparative Analyses of Neotropical-Paleotropical Bamboos

To elucidate chloroplast genome evolution within neotropical-paleotropical bamboos, we fully characterized the chloroplast genome of the woody bamboo Guadua angustifolia. This genome is 135,331 bp long and comprises of an 82,839-bp large single-copy (LSC) region, a 12,898-bp small single-copy (SSC) region, and a pair of 19,797-bp inverted repeats (IRs). Comparative analyses revealed marked conservation of gene content and sequence evolutionary rates between neotropical and paleotropical woody bamboos. The neotropical herbaceous bamboo Cryptochloa strictiflora differs from woody bamboos in IR/SSC boundaries in that it exhibits slightly contracted IRs and a faster substitution rate. The G. angustifolia chloroplast genome is similar in size to that of neotropical herbaceous bamboos but is ~3 kb smaller than that of paleotropical woody bamboos. Dissimilarities in genome size are correlated with differences in the lengths of intergenic spacers, which are caused by large-fragment insertion and deletion. Phylogenomic analyses of 62 taxa yielded a tree topology identical to that found in preceding studies. Divergence time estimation suggested that most bamboo genera diverged after the Miocene and that speciation events of extant species occurred during or after the Pliocene.     

Origins of New World monkeys

Fossil ceboid evidence is reviewed with reference to the origins and affinities of the New World monkeys. This evidence indicates that the ceboids evolved from a North American primate of omomyid-like form. The events of continental drift apparently had little to do with the origin and dispersion of the New World monkeys and direct relationships to the Old World monkeys are not indicated. Three of the five extant New World monkey subfamilies are represented in late Miocene deposits of South America and it appears that evolutionary events leading to extant Ceboidea occurred within the South American continent.     

Genome duplication and the origin of angiosperms

Despite intensive research, little is known about the origin of the angiosperms and their rise to ecological dominance during the Early Cretaceous. Based on whole-genome analyses of Arabidopsis thaliana, there is compelling evidence that angiosperms underwent two whole-genome duplication events early during their evolutionary history. Recent studies have shown that these events were crucial for the creation of many important developmental and regulatory genes found in extant angiosperm genomes. Here, we argue that these ancient polyploidy events might have also had an important role in the origin and diversification of the angiosperms.     

An evolutionary perspective on the regulation of carpel development

The carpel, or female reproductive organ enclosing the ovules, is one of the major evolutionary innovations of the flowering plants. The control of carpel development has been intensively studied in the model eudicot species Arabidopsis thaliana. This review traces the evolutionary history of genes involved in carpel development by surveying orthologous genes in taxa whose lineages separated from that of A. thaliana at different levels of the phylogenetic tree of the seed plants. Some aspects of the control of female reproductive development are conserved between the flowering plants and their sister group, the gymnosperms, indicating the presence of these in the common ancestor of the extant seeds plants, some 300 million years ago. Gene duplications that took place in the pre-angiosperm lineage, before the evolution of the first flowering plants, provided novel gene clades of potential importance for the origin of the carpel. Subsequent to the appearance of the first flowering plants, further gene duplications have led to sub-functionalization events, in which pre-existing reproductive functions were shared between paralogous gene clades. In some cases, fluidity in gene function is evident, leading to similar functions in carpel development being controlled by non-orthologous genes in different taxa. In other cases, gene duplication events have created sequences that evolved novel functions by the process of neo-functionalization, thereby generating biodiversity in carpel and fruit structures.     

Chromosome evolution in new world monkeys (platyrrhini)

During the last decades, New World monkey (NWM, Platyrrhini, Anthropoideae) comparative cytogenetics has shed light on many fundamental aspects of genome organisation and evolution in this fascinating, but also highly endangered group of neotropical primates. In this review, we first provide an overview about the evolutionary origin of the inferred ancestral NWM karyotype of 2n = 54 chromosomes and about the lineage-specific chromosome rearrangements resulting in the highly divergent karyotypes of extant NWM species, ranging from 2n = 16 in a titi monkey to 2n = 62 in a woolly monkey. Next, we discuss the available data on the chromosome phylogeny of NWM in the context of recent molecular phylogenetic analyses. In the last part, we highlight some recent research on the molecular mechanisms responsible for the large-scale evolutionary genomic changes in platyrrhine monkeys.     

生物多样性起源与进化研究进展

生物多样性的起源与进化是生命科学领域最重要的科学问题之一。多组学数据的积累和相关分析技术的发展, 极大地推动了人们对生物多样性起源与进化的理解和研究, 使得阐明生物进化事件发生的过程与机制成为可能。值此《生物多样性》创刊30周年之际, 本文简要回顾生物多样性起源与进化相关研究在近年来取得的重要研究进展, 以期帮助读者了解该研究方向的发展现状。过去10年中, 生物多样性起源与进化相关研究在生命之树重建、生物多样性时空分布格局、物种概念、物种形成与适应性进化以及新性状起源与多样化等方面取得了许多重要进展, 并在此基础上厘清了许多分类单元间的系统发育关系、揭示了生物多样性分布格局的部分历史成因、提出了新的物种概念和物种形成模型、阐明了新性状和新功能发生的部分分子机制。我们认为, 更精准地重建生命之树、深入挖掘基因组数据以及多学科交叉融合将是今后生物多样性研究的主要趋势。     

The Great American Interchange in birds: a phylogenetic perspective with the genus Trogon

The 'Great American Interchange' (GAI) is recognized as having had a dramatic effect on biodiversity throughout the Neotropics. However, investigation of patterns in Neotropical avian biodiversity has generally been focused on South American taxa in the Amazon Basin, leaving the contribution of Central American taxa under-studied. More rigorous studies of lineages distributed across the entire Neotropics are needed to uncover phylogeographical patterns throughout the area, offering insights into mechanisms that contribute to overall Neotropical biodiversity. Here we use mitochondrial DNA sequence data and intensive geographical sampling from the widespread Neotropical avian genus Trogon to investigate the role of the GAI in shaping its phylogeographical history. Our results show that genetic diversity in Trogon exceeds the perceived biodiversity, and that the GAI resulted in lineage diversification within the genus. Despite greater diversity in South America, a Central American centre of origin with multiple and independent dispersals into South America is indicated. These dispersals were followed by the evolution of divergent lineages associated with the Andes Mountains and other South American geographical features. According to our phylogenetic reconstructions, several species, which were originally defined by morphological characters, are nonmonophyletic. In sum, our results elucidate the evolutionary history of Trogon , reveal patterns obscured by extant biodiversity, and serve as a biogeographical model to consider in future studies.     

Extant primitively segmented spiders have recently diversified from an ancient lineage

Living fossils are lineages that have retained plesiomorphic traits through long time periods. It is expected that such lineages have both originated and diversified long ago. Such expectations have recently been challenged in some textbook examples of living fossils, notably in extant cycads and coelacanths. Using a phylogenetic approach, we tested the patterns of the origin and diversification of liphistiid spiders, a clade of spiders considered to be living fossils due to their retention of arachnid plesiomorphies and their exclusive grouping in Mesothelae, an ancient clade sister to all modern spiders. Facilitated by original sampling throughout their Asian range, we here provide the phylogenetic framework necessary for reconstructing liphistiid biogeographic history. All phylogenetic analyses support the monophyly of Liphistiidae and of eight genera. As the fossil evidence supports a Carboniferous Euramerican origin of Mesothelae, our dating analyses postulate a long eastward over-land dispersal towards the Asian origin of Liphistiidae during the Palaeogene (39–58 Ma). Contrary to expectations, diversification within extant liphistiid genera is relatively recent, in the Neogene and Late Palaeogene (4–24 Ma). While no over-water dispersal events are needed to explain their evolutionary history, the history of liphistiid spiders has the potential to play prominently in vicariant biogeographic studies.     

Role of Caribbean Islands in the diversification and biogeography of Neotropical Heraclides swallowtails

Numerous hypotheses on the evolution of Neotropical biodiversity have stimulated research to provide a better understanding of diversity dynamics and distribution patterns of the region. However, few studies integrate molecular and morphological data with complete sampling of a Neotropical group, and so there has been little synthesis of the multiple processes governing biodiversity through space and time. Here, a total‐evidence phylogenetic approach is used to reconstruct the evolutionary history of the butterfly subgenus Heraclides. We used DNA sequences for two mitochondrial genes and one nuclear gene and coded 133 morphological characters of larvae and adults. A robust and well‐resolved phylogeny was obtained using several analytical approaches, while molecular dating and biogeographical analyses indicated an early Miocene origin (22 Mya) in the Caribbean Islands. We inferred six independent dispersal events from the Caribbean to the mainland, and three from the mainland to the Caribbean, and we suggest that cooling climates with decreasing sea levels may have contributed to these events. The time‐calibrated tree is best explained by a museum model of diversity in which both speciation and extinction rates remained constant through time. By assessing both continental and fine‐scale biodiversity patterns, this study provides new findings, for instance that islands may act as source of diversity rather than as a sink, to explain spatio‐temporal macroevolutionary processes within the Neotropical region.     

Simulating trees with a fixed number of extant species

In this paper, I develop efficient tools to simulate trees with a fixed number of extant species. The tools are provided in my open source R-package TreeSim available on CRAN. The new model presented here is a constant rate birth-death process with mass extinction and/or rate shift events at arbitrarily fixed times 1) before the present or 2) after the origin. The simulation approach for case (2) can also be used to simulate under more general models with fixed events after the origin. I use the developed simulation tools for showing that a mass extinction event cannot be distinguished from a model with constant speciation and extinction rates interrupted by a phase of stasis based on trees consisting of only extant species. However, once we distinguish between mass extinction and period of stasis based on paleontological data, fast simulations of trees with a fixed number of species allow inference of speciation and extinction rates using approximate Bayesian computation and allow for robustness analysis once maximum likelihood parameter estimations are available.     

Steady diversification of derived liverworts under Tertiary climatic fluctuations

Tropical forests contain the majority of extant plant diversity and their role as a cradle and/or museum of biodiversity is an important issue in our attempts to assess the long-term consequences of global climate change for terrestrial biomes. Highly diverse groups of liverworts are an often ignored but extremely common element in rainforests, and thus their evolution may shed light on the ecological robustness of rainforest biomes to climate fluctuations. We record a remarkable constant accumulation of diversity through time for the most species-rich family of liverworts, Lejeuneaceae, inferred by divergence time estimates. The observed pattern supports the recently developed concept of a dual role of the tropics as both a museum and a cradle of biodiversity.     

Biotic and environmental dynamics through the Late Jurassic–Early Cretaceous transition: evidence for protracted faunal and ecological turnover

The Late Jurassic to Early Cretaceous interval represents a time of environmental upheaval and cataclysmic events, combined with disruptions to terrestrial and marine ecosystems. Historically, the Jurassic/Cretaceous (J/K) boundary was classified as one of eight mass extinctions. However, more recent research has largely overturned this view, revealing a much more complex pattern of biotic and abiotic dynamics than has previously been appreciated. Here, we present a synthesis of our current knowledge of Late Jurassic–Early Cretaceous events, focusing particularly on events closest to the J/K boundary. We find evidence for a combination of short‐term catastrophic events, large‐scale tectonic processes and environmental perturbations, and major clade interactions that led to a seemingly dramatic faunal and ecological turnover in both the marine and terrestrial realms. This is coupled with a great reduction in global biodiversity which might in part be explained by poor sampling. Very few groups appear to have been entirely resilient to this J/K boundary ‘event’, which hints at a ‘cascade model’ of ecosystem changes driving faunal dynamics. Within terrestrial ecosystems, larger, more‐specialised organisms, such as saurischian dinosaurs, appear to have suffered the most. Medium‐sized tetanuran theropods declined, and were replaced by larger‐bodied groups, and basal eusauropods were replaced by neosauropod faunas. The ascent of paravian theropods is emphasised by escalated competition with contemporary pterosaur groups, culminating in the explosive radiation of birds, although the timing of this is obfuscated by biases in sampling. Smaller, more ecologically diverse terrestrial non‐archosaurs, such as lissamphibians and mammaliaforms, were comparatively resilient to extinctions, instead documenting the origination of many extant groups around the J/K boundary. In the marine realm, extinctions were focused on low‐latitude, shallow marine shelf‐dwelling faunas, corresponding to a significant eustatic sea‐level fall in the latest Jurassic. More mobile and ecologically plastic marine groups, such as ichthyosaurs, survived the boundary relatively unscathed. High rates of extinction and turnover in other macropredaceous marine groups, including plesiosaurs, are accompanied by the origin of most major lineages of extant sharks. Groups which occupied both marine and terrestrial ecosystems, including crocodylomorphs, document a selective extinction in shallow marine forms, whereas turtles appear to have diversified. These patterns suggest that different extinction selectivity and ecological processes were operating between marine and terrestrial ecosystems, which were ultimately important in determining the fates of many key groups, as well as the origins of many major extant lineages. We identify a series of potential abiotic candidates for driving these patterns, including multiple bolide impacts, several episodes of flood basalt eruptions, dramatic climate change, and major disruptions to oceanic systems. The J/K transition therefore, although not a mass extinction, represents an important transitional period in the co‐evolutionary history of life on Earth.     

Mitochondrial DNA from prehistoric canids highlights relationships between dogs and South-East European wolves

The question of the origins of the dog has been much debated. The dog is descended from the wolf that at the end of the last glaciation (the archaeologically hypothesized period of dog domestication) was one of the most widespread among Holarctic mammals. Scenarios provided by genetic studies range from multiple dog-founding events to a single origin in East Asia. The earliest fossil dogs, dated approximately 17-12,000 radiocarbon ((14)C) years ago (YA), were found in Europe and in the Middle East. Ancient DNA (a-DNA) evidence could contribute to the identification of dog-founder wolf populations. To gain insight into the relationships between ancient European wolves and dogs we analyzed a 262-bp mitochondrial DNA control region fragment retrieved from five prehistoric Italian canids ranging in age from approximately 15,000 to approximately 3,000 (14)C YA. These canids were compared to a worldwide sample of 547 purebred dogs and 341 wolves. The ancient sequences were highly diverse and joined the three major clades of extant dog sequences. Phylogenetic investigations highlighted relationships between the ancient sequences and geographically widespread extant dog matrilines and between the ancient sequences and extant wolf matrilines of mainly East European origin. The results provide a-DNA support for the involvement of European wolves in the origins of the three major dog clades. Genetic data also suggest multiple independent domestication events. East European wolves may still reflect the genetic variation of ancient dog-founder populations.